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Effect of different biofloc system on water quality,

biofloc composition and growth performance in

Litopenaeus vannamei (Boone, 1931)

Muthusamy Rajkumar1, Pramod Kumar Pandey2, Radhakrishnapillai Aravind2, Alagarsamy

Vennila3, Vivekanand Bharti1 & Chandra Sekharan Purushothaman1

1Central Marine Fisheries Research Institute, Cochin, Kerala, India2Central Institute of Fisheries Education, Versova, Mumbai, Maharashtra, India3Sugarcane Breeding Institute, Coimbatore, Tamilnadu, India

Correspondence: M Rajkumar, Central Marine Fisheries Research Institute, Cochin, Kerala 682018, India. E-mail: rajfcri@gmail.

com

Abstract

The experiment was conducted with three biofloc

treatments and one control in triplicate in 500 L

capacity indoor tanks. Biofloc tanks, filled with

350 L of water, were fed with sugarcane molas-

ses (BFTS), tapioca flour (BFTT), wheat flour

(BFTW) and clean water as control without biofloc

and allowed to stand for 30 days. The postlarvae

of Litopenaeus vannamei (Boone, 1931) with an

Average body weight of 0.15 � 0.02 g were

stocked at the rate of 130 PL m�2 and cultured

for a period of 60 days fed with pelleted feed at

the rate of 1.5% of biomass. The total suspended

solids (TSS) level was maintained at around

500 mg L�1 in BFT tanks. The addition of carbo-

hydrate significantly reduced the total ammonia-

N (TAN), nitrite-N and nitrate-N in water and it

significantly increased the total heterotrophic bac-

teria (THB) population in the biofloc treatments.

There was a significant difference in the final

average body weight (8.49 � 0.09 g) in the

wheat flour treatment (BFTW) than those treat-

ment and control group of the shrimp. Survival

of the shrimps was not affected by the treatments

and ranged between 82.02% and 90.3%. The

proximate and chemical composition of biofloc

and proximate composition of the shrimp was sig-

nificantly different between the biofloc treatments

and control. Tintinids, ciliates, copepods, cyano-

bacteria and nematodes were identified in all the

biofloc treatments, nematodes being the most

dominant group of organisms in the biofloc. It

could be concluded that the use of wheat flour

(BFTW) effectively enhanced the biofloc production

and contributed towards better water quality

which resulted in higher production of shrimp.

Keywords: biofloc, Litopenaeus vannamei, total

heterotrophic bacteria, water quality, carbohy-

drate

Introduction

Crustaceans have high demand and economic value

both in domestic and international markets.

According to the Food and Agriculture Organiza-

tion (2003, 2008), shrimp is the most important

and profitable commodity among all seafood trades.

Shrimp culture has a significant exploration among

farmers, contributing to world’s aquaculture pro-

duction, but concerns about the environmental

impacts due to this activity have also increased

(Tovar, Moreno, Manuel-Vez & Garcia-Vargas

2000; Jory, Cabrera, Dugger, Fegan, Lee, Lawrence,

Jackson, Mcintosh & Castaneda 2001). Aquaculture

systems mainly depend on the exploitation of auto-

trophic and heterotrophic microbial food webs. Het-

erotrophic food web consists of decomposition of

organic matter by microorganisms, leading to the

formation of assimilable detritus and inorganic

nutrients. The detritus and associated microbes are

directly consumed by the cultured animals or by

other small animals on which the cultured species

feed (Moriarty 1997). The heterotrophic food web

consistently appears as a major contributor to the

total production of the target animals (Schroeder

1987). The shrimps assimilate only 15–30% of the

© 2015 John Wiley & Sons Ltd 1

Aquaculture Research, 2015, 1–13 doi:10.1111/are.12792

nitrogen added in the feed in a pond environment,

the remaining quantity is lost to the system as

ammonia and organic-N in the form of faeces and

feed residue. The organic-N in faeces and uneaten

feed undergoes decomposition resulting in ammonia

production. Therefore, a high protein level in

shrimp feed contribute to high concentration of

ammonia in the water column which is detrimental

to the cultured animals, and needs to be minimized.

To rectify the above mentioned constraints, the bio-

floc technology (BFT) systems were developed to

minimize effluent discharge, protect the surround-

ing water bodies and improve farm bio-security

(Burford, Thompson, McIntosh, Bauman & Pearson

2003; Avnimelech 2007).

Farming of L. vannamei is generally conducted

extensively in grow-out ponds, and has been devel-

oped in indoor high-intensive farming system to

meet the growing world demand (Lin, Shan, Liu &

Huang 2001; Zhou 2001). With rapid expansion

and intensification, however, there is also a growing

concern about the ecological sustainability of

shrimp farming (Naylor, Goldburg, Primavera, Ka-

utsk, Beveridge, Clay, Folke, Lubchencoi, Mooney &

Troell 2000). The cultured shrimps retain only 20–30% of feed nutrient; therefore, 70–80% of high die-

tary protein is excreted and accumulated in water,

which leads to deterioration of water quality (Av-

nimelech & Ritvo 2003). Moreover, deteriorated

water quality has resulted in disease outbreaks and

heavy financial losses (Samocha, Lawrence, Collins,

Castille, Bray, Davies, Lee & Wood 2004). Such

environmental issues have created a large demand

for productive, efficient and sustainable shrimp

farming systems that have low impact on the envi-

ronment and are more likely to be disease free

(Horowitz & Horowitz 2001). Hari, Kurup, Vargh-

ese, Schrama and Verdegem (2004, 2006) reported

addition of tapioca flour into Penaeus monodon cul-

ture system can significantly reduce the TAN and

NO2-N concentrations. Samocha, Patnaik, Speed,

Ali, Burger, Almeida, Ayub, Harisanto, Horowitz

and Brock (2007) reported that the molasses addi-

tion does not result in a significant effect on L. van-

namei culture system. Asaduzzaman, Wahab,

Verdegem, Huque, Salam and Azim (2008) reported

that the addition of tapioca flour into Macrobrachi-

um rosenbergii culture system can result in a signifi-

cant decrease in the TAN and NO2-N

concentrations. Although, the possibilities of utiliz-

ing tapioca as a carbohydrate source in animal feed

formulations and induce biofloc for shrimp produc-

tion has been established, the feed manufacturers

and shrimp farmers have not incorporated cassava

because of its high cost as compared with other

cheap carbohydrate sources. Wheat is one of the

cheap carbohydrate sources in India.

Therefore, the study aims to develop microbial

biofloc for culture of L. vannamei by using carbo-

hydrate materials (sugarcane molasses, tapioca

flour and wheat flour) as a carbon source to boost

the production by improving the conversion of

nutrients into harvestable products while main-

taining good water quality. The objectives of the

study were: (1) to assess the effect of biofloc on

the water quality, (2) to assess the effect of biofloc

on growth of L. vannamei and (3) to investigate

the effects of carbon source/C:N ratio of feed on

proximate composition of biofloc.

Materials and methods

Experimental design

The experiment was conducted at Wet Laboratory

of the Central Institute of Fisheries Education (CIFE),

Versova, Mumbai, India. Uniform-size Fiberglass

Reinforced Plastic (FRP) circular tanks of 500 L

capacity with 0.98 m diameter, filled with 350 L of

water were used for the experiment. Three treat-

ments with a control in triplicates were set up using

completely randomized design (CRD). Three treat-

ments were biofloc tank fertilized with sugarcane

molasses (BFTS), tapioca flour (BFTT) and wheat

flour (BFTW). All the treatments and control were

fed with commercially available feed [Charoen

Pokph (CP) and (India) Pvt. Ltd, Chennai, India]

having 34.5% crude protein twice a day. The aera-

tion (7 mg L�1) was provided in all the experimen-

tal tanks from a centralized aeration unit. The

aeration pipe in each tank was provided with an air

stone and a regulator to control the air pressure in

all the tanks.

The seawater was pumped from the Aksa Beach

(Mumbai, India) during high tide time. The col-

lected seawater was stored in the 5000 L reservoir

tank. The seawater was allowed to settle down for a

week and was diluted with tap water to achieve a

salinity of 25 g L�1. The 350 L of diluted seawater

(25 g L�1) was filled in each of the experimental

tanks. The biofloc was produced using (25 g L�1) in

500 L capacity tanks before stocking of the postlar-

vae. Sugarcane molasses, tapioca flour and wheat

flour which contain 69–76 % nitrogen-free extracts

© 2015 John Wiley & Sons Ltd, Aquaculture Research, 1–132

Effect of biofloc on growth of L. vannamei M Rajkumar et al. Aquaculture Research, 2015, 1–13

was used as carbohydrate source. The sugarcane

molasses were prepared by fermenting boiled sugar-

cane juice with yeast (Saccharomyces cerevisiae) for

2 days. After 2 days, it was used as an input for bio-

floc production. Twenty gram of carbohydrate was

added per gram of TAN released. The amount of

TAN released was estimated assuming that added

carbohydrate contains 50% carbon and that 50% of

the dietary protein input was converted to ammo-

nia. In consequence, 0.53 kg each carbon was

applied for each kg of the 34.5% dietary protein feed

administrated. The photoperiod was maintained at

12-h dark and 12-h light for the whole experimen-

tal period.

Stocking of shrimp seed and tank management

The specific pathogen free (SPF) L. vannamei

(PL9) seeds were procured from Madha Hatchery,

Chennai, India. The postlarvae were acclimatized

in 500 L tanks for 2 weeks before being stocked

in the experimental tanks. The juveniles

(0.15 � 0.02 g) were stocked when bioflocs mea-

sured as total suspended solids (TSS) and floc vol-

ume was higher than 100 mg L�1 and between

5 and 50 mL respectively. The shrimps were

stocked in 30 day old biofloc treatments and con-

trol tanks at the rate of 130 PL m�2. Tanks were

aerated with an air pump to maintain dissolved

oxygen content at saturation level. CP manufac-

tured pelleted feeds (1.8–3.0 mm) were used for

feeding throughout the experiment. Biochemical

composition of the experimental diet and the car-

bon sources are given in Table 1. Feeding rates

were based on observation of feeding behaviour

of shrimp in the biofloc treatments during first

few days and fixed at 1.5% of the total stocked

biomass daily, and adjusted fortnightly after

weighing shrimp sample. The same amount of

feed was fed in all the treatment and control

tanks. Daily feed rations were split into two equal

quantities and fed at 08:00 and 17:00 hours in

all the tanks. The shrimps were cultured for

60 days. When the pH of water dropped below

7.0, NaHCO3 was added to raise the pH to 7.5.

Addition of freshwater to compensate evaporation

loss and removal of floc was carried out on a

weekly basis.

Water quality parameters

Water samples were collected at fortnightly inter-

vals from the experimental tanks during morning

hours between 8:00 and 9:00 hours for a period

of 90 days. Temperature (H-9283; Shenzhen Vici-

meter Technology Co. Ltd., Shenzhen, Guangdong,

China), pH (Eutech Instruments, klang, Selangor

D.E., Malaysia) and electrical conductivity (EC)

(Eutech Instruments) were measured in the experi-

mental unit itself. Dissolved oxygen and biochemi-

cal oxygen demand (BOD5) measured by following

APHA (2005) guidelines for sample collection and

preservation. Total alkalinity and total hardness of

water were measured volumetrically (APHA

2005). Water samples were collected from each

tank and filtered under vacuum pressure through

pre-dried and pre-weighed GF/C filter paper. The

filtered water was used for nutrient analysis and

the filter paper for the estimation of total sus-

pended solid (APHA 2005). Total ammonia-nitro-

gen (TAN), nitrite (NO2-N) and nitrate (NO3-N)

were analysed spectrophotometrically following

APHA (2005). The weight difference of the dried

sample before and after ignition was taken for cal-

culation of volatile suspended solids (VSS). Floc

volume (FV) was measured by using the Imhoff

Cone (Merck Specialties, Mumbai, India). Floc-mor-

phostructure was observed using biological micro-

scope and photographed with camera (JVC Color

Video Camera, TK-C1481BEG, Victor Company,

Yokohama, Japan) attached to microscope

(H600L; Hund GMBH, Wetzlar, Germany). Chloro-

phyll a was measured following trichromatic

method (APHA 2005) using spectrophotometer

(Thermospectronic, UV 1, Cambridge, UK).

Total heterotrophic bacteria (THB) were enumer-

ated on R2A agar medium{Enzymatic Digest of

Table 1 Biochemical composition of the experimental

feed and carbon sources

Constituent (%) Feed

Carbon source

Sugarcane

molasses

Tapioca

flour

Wheat

flour

Crude Protein 34.50 6.30 11.46 14.72

Ether Extract 13.27 4.01 3.19 3.25

Crude Fibre 4.27 3.75 6.16 5.15

Total Ash 10.80 16.20 5.10 2.42

Nitrogen-free Extract 37.16 69.74 74.04 74.46

Moisture 5.35 22.67 8.26 6.64

Carbon Nitrogen

ratio

7.68 17.43 10.11 9.40

Values are in dry weight basis.

© 2015 John Wiley & Sons Ltd, Aquaculture Research, 1–13 3

Aquaculture Research, 2015, 1–13 Effect of biofloc on growth of L. vannamei M Rajkumar et al.

Casein (0.25 g), Protease Peptone (0.25 g), Acid

Hydrolysate of Casein (0.5 g), Yeast Extract (0.5 g),

Dextrose (0.5 g), Soluble Starch (0.5 g), Dipotassi-

um Phosphate (0.3 g), Magnesium Sulphate Hepta-

hydrate (0.05 g), Sodium Pyruvate (0.3 g), Agar

(15 g) and Final pH: 7.2 � 0.2 at 25°C from all

the treatment tanks following spread plate method.

The inoculated plates were incubated at 37°C for

48 h and the THB is expressed as colony forming

unit per millilitre (CFU mL�1).

Proximate composition of biofloc and shrimps

Biofloc samples were collected for biochemical

analysis at the end of the experiment from each

tank using 100-lm mesh and were dried in an

oven at 60°C. The dried samples were ground

and processed for biochemical analysis following

AOAC (2005). For moisture contents the known

quantity of samples were dried in an oven at

105°C until constant weight obtained. The differ-

ence in the weight before and after drying of

sample was taken and expressed in percentage.

For ash contents, a known quantity of dry sam-

ple was burnt in a muffle furnace at 550°C for

4 h and the ash was cooled and weighed. The

crude protein content was determined by the

Kjeldahl method (KEL Plus – Classic DX VA, Peli-

can Equipments, Chennai, Tamil Nadu, India),

Crude lipid by automatic fat extraction system

(SOCS PLUS-SCS 08 AS, Pelican Equipments,

Chennai, Tamil Nadu, India), crude fibre by auto-

matic fibre analysis system (FIBROTRON-FRB 8,

Tulin Equipments, Chennai, Tamil Nadu, India)

and Nitrogen-free extract was estimated by the

difference (Tacon 1990). The gross energy con-

tent of biofloc sample was determined by using

bomb calorimeter (Parr Calorimetric Thermo-

meter-6772, Parr Instruments, Moline, IL, USA)

and C:N ratios were determined using CHNS ana-

lyser (ElementarAnalysysteme GmbH, Hanau, Ger-

many). Similarly, the biochemical composition of

all the experimental shrimps was estimated after

harvesting.

Growth parameters of shrimp

The sampling was performed at fortnightly interval

to assess the body weight of the shrimps. Shrimps

were starved overnight before taking the weight.

Twenty per cent of the test animals were ran-

domly weighed for all the treatments. The weight

was measured using an electronic balance.

Shrimps were harvested at the end of the

experiment after draining the tanks. Survival rate,

average body weight (ABW), specific growth rate

(SGR), protein efficiency ratio (PER) and total

weight gain were calculated according to the

formulae given below:

Total weight gain (wet weight, g)¼ final weight (g)� initial weight (g)

ABW (g) ¼ total weight (g)=

total Number of animals

SGR ¼ ½ðln final weight� ln initial weightÞ� 100�=no. of days of experiment

PER ¼ net weight gain (wet weight) (g)=

protein consumed (g)

Biochemical composition of biofloc

The biofloc samples were digested using supra

pure concentrated acids (Merck Specialities Pvt.

Ltd., Mumbai, Maharashtra, India), in a micro-

wave-based digestion system (Multiwave 3000;

Anton Parr, Suite, Houston, TX, USA). Three

replicates of 0.250 g of biofloc samples were

taken in the microwave digestion vessels, to

which 5 mL of conc. HNO3, 2 mL of conc. HCl

and 1 mL of conc. HF were added. The vessels

were capped and heated in the microwave unit

at 1200 W to a temperature of 190°C for

30 min at a pressure of 25 bars. The digested

samples were diluted to 50 mL and were used

for the analysis of total phosphorus following

ascorbic acid method APHA (2005). The digested

biofloc samples were used for the analysis of

sodium and potassium using flame photometer

(Elico CL 378, Hyderabad, India) and analysed

five elements (Ca, Mg, Zn, Cu and Fe) by atomic

absorption spectrophotometer (AAnalyst 800;

Perkin Elmer, Waltham, MA, USA) using flame

atomization.

Taxonomic composition of biofloc

The plankton samples were collected in triplicate

and concentrated to 50 mL by filtering the water

using bolting silk cloth (no. 25) from the treat-

ment tanks. The collected plankton samples were

preserved in 5% formalin for further analyses



(Pennak 1978). The counting of plankton was

carried out using a Sedgwick-Rafter counting cell

following APHA (2005). The averages of three

samples were taken into consideration and the

results are given in terms of cells per litre. The

photographs of all the major planktons were taken

using a camera (JVC Color Video Camera, TK-

C1481BEG) attached to Hund microscope (H600L;

HundWetzlar). The morphometric features of the

organisms were measured using the Bio-wizard

software. Organisms were identified using keys

and monographs given by Graham, Graham and

Wilcox (2008).

Statistical analysis

All statistical analyses were performed using SAS

v9.3 for Windows (Cary, NC, USA). Water quality

parameters were compared by two-way repeated

measures ANOVA with treatment as main factor and

sampling date as repeated measures factor. One-

way analysis of variance (ANOVA) was performed to

examine difference of growth parameters, bio-

chemical composition of shrimp and nutritional

quality of biofloc among the treatments and con-

trol. The analyses were run at 5% significance

level.

Results


The biofloc development was observed in terms of

FV and TSS. The FV and TSS gradually increased

during the experiment. Bioflocs were observed as

brown in colour, and were composed of suspended

organic particles in the form of flocculated aggre-

gates, which were colonized by a number of het-

erotrophic bacteria, microalgae and protozoa. All

the water quality parameters in the three experi-

mental tanks were found within suitable ranges

for L. vannamei culture throughout the experimen-

tal period. There were no significant differences

(P > 0.05) among the treatments in terms of

water temperature, pH, alkalinity, electrical con-

ductivity and total hardness (Table 2). All other

parameters showed significant variation

(P < 0.05) among the treatments. The treatment,

BFTS (5.99 mg L�1) had significantly lower DO

than that of control and other treatments. The

TAN, nitrite-N and nitrate-N concentrations in

control were significantly higher than those of bio-

floc treatments except TAN in BFTS. The treat-

ments BFTT and BFTW showed significantly higher

TSS, VSS, BOD, chlorophyll and plankton density

Table 2 Water quality parameters of different experimental groups

Parameter Control

Treatment

BFTS BFTT BFTW

Temperature (°C) 23.29 � 0.24 23.12 � 0.20 23.08 � 0.20 23.16 � 0.23

Alkalinity (mg CaCO3 L�1) 138.89 � 8.11 153.52 � 10.91 150.61 � 9.39 138.68 � 9.43

pH (no unit) 7.8 � 0.0 7.8 � 0.0 7.6 � 0.0 7.7 � 0.0

Hardness (mg CaCO3 L�1) 4635.85 � 84.16 4261.36 � 200.10 4456.11a � 152.01 4453.97 � 109.59

Dissolved oxygen (mg L�1) 6.57 � 0.43ab 5.99 � 0.26b 6.70 � 0.36ab 7.39 � 0.44a

Total ammonia-nitrogen (mg L�1) 0.78 � 0.10a 0.57 � 0.10ab 0.40 � 0.08bc 0.24 � 0.05c

Nitrite-N (mg L�1) 1.89 � 0.14a 0.93 � 0.09b 0.75bc � 0.11 0.61c � 0.05

Nitrate-N (mg L�1) 3.21 � 0.14a 2.42 � 0.12bc 2.56 � 0.12b 2.09 � 0.12c

Total suspended solids (mg L�1) 158.5 � 29.66b 285.08 � 36.73b 493.50 � 69.31a 484.94 � 65.46a

Volatile suspended solids (mg L�1) 282.00 � 42.54b 427.83 � 51.93ab 494.89 � 56.15a 526.22 � 59.21a

Electrical conductivity (mS cm�1) 33.39 � 2.09a 31.60 � 2.47a 46.73 � 21.23a 37.64 � 1.82a

Chlorophyll a (lg L�1) 283.44 � 39.41b 439.14 � 49.13a 516.77 � 64.30a 553.67 � 59.99a

Biological oxygen demand (mg L�1) 15.98 � 2.42c 64.34 � 15.16b 77.54 � 17.58ab 108.44 � 16.25a

Floc volume (mg L�1) 15.50 � 1.75c 32.17 � 2.88b 33.64 � 3.25b 43.06 � 3.60a

Total beterotrophic bacteria 9106

(CFU mL�1)

19.40 � 139.57b 93.50 � 107.23ab 131.88 � 107.69a 148.16 � 118.00a

Plankton 9106 (cells L�1) 1.45 � 0.08b 1.93 � 0.23ab 2.23 � 0.18a 2.38 � 0.21a

BFTS, sugarcane molasses; BFTT, tapioca flour; BFTW, wheat flour.

The values are means (�SE, n = 18) of three replications in six sampling date for the treatment and control. Mean values in the

same row with different superscript differ significantly (P < 0.05).



than the control. The parameters, VSS, chloro-

phyll, THB and plankton density in BFTS was on

par with those of BFTT and BFTW. Among the

treatments, BFTW and BFTT, floc volume in BFTWwas significantly higher than that of BFTT.

Growth parameters

There was a significant difference (P < 0.05) in

the ABW, growth rate, PER and SGR among the

treatments and control. There were no significant

differences in the survival rate. The ABW, growth

rate, PER and SGR of shrimps in BFTW treatment

was significantly higher than those of other biofloc

treatments and control. The total weight gain was

also significantly (P < 0.05) higher in BFTW than

that of other treatments and control (Table 3).

Proximate and biochemical composition of biofloc

The parameters, crude protein, ether extract, crude

fibre and GE content of biofloc in BFTW were sig-

nificantly higher than those of control. The mois-

ture, ash and total carbon contents in control

were significantly lower than those of BFTW. The

C:N ratio of the treatments BFTT and BFTW was

on par and significantly higher than that of BFTSand control (Table 4). There was a significant dif-

ference in the biochemical composition among the

biofloc treatments and control. There was a signifi-

cant difference in the nutrient composition among

biofloc treatments and control. The concentration

of Fe and Ca was significantly higher in BFTT than

that of other treatments, whereas, the concentra-

tion of Mg, Na and K was significantly higher in

BFTW than that of others (Table 5).

Biochemical composition of shrimp reared in

biofloc-based system

There was a significant difference (P < 0.05) in the

crude protein in the treatment BFTS among the

treatments. The treatment, BFTW had significantly

higher ether extract than that of BFTS and control

Table 3 Growth parameters of shrimp in different biofloc treatments and the control (means � SE)

Parameters Control

Treatment

BFTS BFTT BFTW

Average body weight (g) 5.97 � 0.03d 6.64 � 0.13c 7.25 � 0.09b 8.49 � 0.09a

Growth rate (g day�1) 0.06 � 0.00d 0.07 � 0.001c 0.08 � 0.002b 0.09 � 0.001a

Specific growth rate 4.10 � 0.03d 4.25 � 0.04c 4.43 � 0.02b 4.57 � 0.03a

Protein efficiency ratio 1.58 � 0.01d 2.16 � 0.03c 2.34 � 0.03b 2.59 � 0.08a

Survival (%) 86.90 � 3.8a 82.2 � 3.4a 85.6 � 3.5a 90.3 � 0.96a

Total weight gain (g) 623.00 � 12.99c 656.08 � 27.14c 744.63 � 37.64b 919.41 � 14.76a


Mean values in the same row with different superscript differ significantly (P < 0.05).

Table 4 Proximate composition of bioflocs (mean � SE) produced in shrimp feeding experiment with of bioflocs

Parameter (%) Control

Treatment

BFTS BFTT BFTW

Moisture 74.34 � 5.43a 63.51 � 2.14ab 63.74 � 2.51ab 56.51 � 3.12b

Ash 29.03 � 0.93a 22.53 � 0.22c 14.88 � 0.46d 25.04 � 0.39b

Crude protein 25.29 � 0.75c 45.98 � 0.59b 52.03 � 1.57a 53.65 � 0.7a

Ether extract 0.48 � 0.09b 0.57 � 0.07b 0.70 � 0.03ab 0.92 � 0.003a

Crude fibre 11.88 � 1.10c 12.92 � 0.8bc 15.25 � 0.06ab 16.65 � 0.02a

Carbon 45.20 � 1.77a 30.92 � 0.45b 32.39 � 1.93b 20.39 � 0.45c

Carbon nitrogen ratio 12.35 � 0.06c 7.2 � 0.08b 6.52 � 0.16a 6.011 � 0.14a

Gross energy* 19.42 � 1.02c 22.45 � 0.56c 25.4 � 1.25b 27.25 � 0.86a



*Values expressed in kJ g�1.



and was at par with BFTT. The treatment BFTW had

significantly higher crude fibre than that of control

and was at par with BFTS and BFTT control and

was at par with BFTT (Table 6).


In the bioflocs treatment group, floc was seen in

anomalous flocculation with bacteria and zoo-

plankton especially nematodes (Fig. 1). However,

in the relative control group, there were a few of

detritus and sloughs in the sediment of the Imhoff

cone. The taxonomic compositions of different floc-

associated planktonic organisms are given in

Fig. 2. The group of organisms was identified as

tintinids, ciliates, copepods, cyanobacteria and

nematodes. Nematodes were the most dominant

group in all the biofloc treatment tanks. The total

number of organisms was significantly high in the

BFTW followed by BFTT and control. These micro-

organisms were found to be grazing on the flocs,

when fresh samples were observed under micro-

Table 5 Biochemical composition (dry weight basis) of biofloc in different treatments and control (means � SE, n = 9)

Parameter

(mg kg�1) Control

Treatment

BFTS BFTT BFTW

Iron 4918.33 � 69.17b 4417.33 � 45.04c 11200 � 179.50a 4479 � 204.86bc

Zinc 161.5 � 0.43b 146.2 � 0.40c 200.77 � 0.26a 200.63 � 0.58a

Magnesium 3537 � 7.77d 7315 � 61.582b 6302.33 � 10.14c 12300 � 124.23a

Potassium 5773.87 � 60.84c 6162.7 � 75.51b 6057.21 � 66.93b 7982.96 � 58.83a

Phosphorous* 14 � 2.00b 23.8 � 1.20ab 27 � 3.0a 31.5 � 3.50a

Calcium* 18.9 � 1.04c 23.9 � 3.78b 37.1 � 3.66a 22.7 � 2.070b

Sodium* 15.45 � 2.73b 16.52 � 1.91a 15.71 � 1.81b 16.81 � 1.82a



*Values expressed in mg g�1.

Table 6 Proximate composition of

L. vannamei cultured in different bio-

floc treatments and control (%

means � SE, n = 3) at the end of

the experiment

Parameter (%) Control

Treatment

BFTS BFTT BFTW

Moisture 76.82 � 0.78 76.20 � 0.14 75.91 � 2.38 78.53 � 2.0

Ash 2.24 � 0.15 2.26 � 0.56 2.21 � 0.07 2.19 � 0.11

Crude protein 20.12c � 0.18 20.07c � 0.73 21.62b � 0.06 20.96a � 2.0

Ether extract 1.39c � 0.18 1.31c � 0.41 1.28b � 0.58 1.25a � 0.29

Crude fibre 1.08b � 0.31 1.06b � 0.3 0.98a � 0.12 1.01a � 0.14

Carbon 44.55a � 0.3 44.3a � 1.25 36.78b � 0.6 31.15c � 2.16


Values are expressed on wet weight basis. Mean values in the same row with dif-

ferent superscript differ significantly (P < 0.05).

(a) (b)

Figure 1 Morphology of floc

under microscope (a) biofloc parti-

cle flocculation with filamentous

algae and bacteria (b) biofloc floc-

culates with nematodes.



scope. In all the biofloc treatment tanks, mostly

the zooplanktons were dominant and very limited

number of phytoplankton could be visualized

under the microscope. The only one phytoplank-

ton (Spirulina sp.) was observed along with zoo-

plankton.

Discussion


The lowest level of dissolved oxygen observed in

this study (4.07 mg L�1) is sufficient for good sur-

vival and growth of L. vannamei (McGraw, Teic-

hert-Coddington, Rouse & Boyd 2001). The

sufficient DO level in all the treatments during the

experiment period is attributed to continuous aera-

tion in biofloc tanks. The water hardness (CaCO3)

and alkalinity levels were above the recommended

levels of 4200 and 130 mg L�1 respectively (Boyd,

Thunjai & Boonyaratpalin 2002), and might

therefore, have provided the physiological condi-

tions allowing shedding and proper formation of

the exoskeleton, promoting growth and survival of

organisms (McGraw & Scarpa 2003).

Concentrations of TAN and nitrite-N, recorded

during the experiment, were at optimum levels as

recommended for juveniles of Pacific white

shrimp (Lin & Chen 2003; Samocha et al. 2004).

The low concentrations of nitrite-N, observed dur-

ing the culture period, suggest oxidation of

ammonia to nitrate (Cohen, Samocha, Fox,

Gandy & Lawrence 2005). Studies evaluating

water quality in zero-exchange systems report

low concentrations of ammonia and nitrite (Bur-

ford, Thompson, McIntosh, Bauman & Pearson

2004; Wasielesky, Atwood, Stokes & Browdy

2006; Ray, Lewis, Browdy & Leffler 2010; Vina-

tea, Galvez, Browdy, Stokes, Venero, Haveman,

Lewis, Lawson, Shuler and Leffler (2010)), result-

ing from the removal of these compounds by

microbial community (Ebeling, Timmons & Bisog-

ni 2006). The assimilation of nitrogen is also evi-

denced from the significantly higher crude protein

content observed in the biofloc of the treatments.

Avnimelech (2007), with the help of a series of

(a) (b) (c) (d)

(e) (f) (g) (h)

(l)(k)(j)(i)

Figure 2 Common zooplankton and phytoplankton observed in the biofloc treatments (a) Tintinids, (b and c)

Ciliates, (d–j) Copepods, (k) Spirulina, (l) Nematodes.



experiments, proved that addition of carbohydrate

reduces the need of dietary protein concentration

and also decrease the TAN level in the system. In

this experiment, the wheat and tapioca flour sig-

nificantly reduced the TAN level when compared

with control.

The presence of high concentration of NO3-N in

BFT treatments indicates the occurrence of nitrifi-

cation processes in the culture systems. While

NO2-N concentration in BFT treatments seems to

be relatively stable, the opposite was observed in

the control which could be explained by the high

rate of nitrification processes in these treatments.

For the first 60 days of the experiment, NO3-N

accumulation was observed in all the biofloc treat-

ments and control which were followed by a sharp

decline on 75th day. This decrease probably

relates to NO3-N uptake by microbes in the

treatments in particular when there was limited

availability of ammonia-nitrogen in the water

(Hargreaves 1998). As most of the ammonia in

the culture system is taken up by heterotrophic

bacteria, the availability of NO3-N in BFT system

thus allows the phytoplankton to grow (Middel-

burg & Nieuwenhuize 2000). Nitrogenous constit-

uents were at safe levels for ammonia (Kuhn,

Lawrence, Boardman, Patnaik, Lori Marsh & Flick

2010), nitrite (Lin & Chen 2003) and nitrate

(Wickins 1976) in the biofloc treatments and con-

trol which are suitable for shrimp culture.

The TSS, observed in this study, was within the

recommended level of <500 mg L�1 for penaeid

shrimps (Samocha et al. 2007). Several authors

have indicated that a similar trend of concentration

of TSS and VSS which is beneficial to the shrimp

and to the system stability (Schryver, Crab, Defoirdt,

Boon & Verstraete 2008; Baloia, Arantes, Schveit-

zer, Magnotti & Vinatea 2013). The EC value was

recorded in the range of 31.60–46.73 mS cm�1

which is within permissible range for shrimp aqua-

culture (Araneda, Perez & Gasca-Leyva 2008). The

decrease in the concentrations of chlorophyll a dur-

ing the study is probably associated with the use of

carbon sources to control ammonia. The use of car-

bon sources in biofloc systems promotes succession

and dominance of bacteria over microalgae (Gonz-

alez-Felix, Ponce-Palafox, Valenzuela-Quinonez, Ar-

redondo-Figueroa & Garcia-Ulloa 2007; Ju, Forster,

Conquest, Dominy, Kuo & Horgen 2008). Chloro-

phyll a concentrations was (553.67 lg L�1) lower

than those reported (Burford et al. 2004; Decamp,

Conquest, Cody, Forster & Tacon 2007) for pacific

white shrimp production biofloc systems. The BOD,

potentially high in the biofloc tanks due to

increased level of microbial density, led to decreased

oxygen availability for shrimp (Azim & Little 2008).

Floc volume levels increased gradually during the

experimental period and the fluctuation over the

time was consistent. The floc development in the

first 30 days was slow due to the clean surfaces of

the tank. The development of adhesiveness of the

biofloc would develop slowly in the initial period.

The recorded level of floc volume (50 mL) was suffi-

cient for the growth of shrimp (Avnimelech 2012).

If the floc volume is higher than 50 mL will leads to

the depletion of DO during morning time. To avoid

that, in this study the floc volume was maintained

at the required level by adding water. The total het-

erotrophic bacterial count in the BFTW was higher

than that reported (Burford et al. 2003). Burford

et al. (2004) reported that the plankton density in

the zero water exchange system was 104 cells

mL�1. The plankton density was very low in all the

treatments due to the limited light and the presence

of carbon source. The results show application of

carbon source enhances the microbial growth

rather than microalgae.


Zooplankton was highly abundant throughout the

study in all the biofloc treatment tanks. Nema-

todes, ciliates and copepods were present in low

abundance at the beginning of the study and

became less due to grazing by the shrimp. Nema-

todes and copepods were seen almost exclusively

grazing on and within the particles and cyanobac-

teria were also principally located within biofloc.

Shrimp might have consumed a portion of the zoo-

plankton community. Previous authors have

shown that these nutritious planktons are an

important food item for shrimp (Moss, Divakaran

& Kim 2001). In terms of potential nutrition, a

decrease in the abundance of zooplankton might

not be desirable for the shrimp. Phytoplankton

abundance was limited in all the biofloc treat-

ments due to the light limitation and carbon

source application. The similar types of plankton

community were observed by Ray et al. (2010).

Growth parameters

Growth rate and final individual shrimp weight

were significantly higher in the treatment BFTW



than those of others. Although no significant dif-

ferences were observed on survival but there were

significant differences in ABW, SGR and PER

between the biofloc and control treatments, indi-

cating that the appropriate quantity of carbohy-

drate addition was helpful in good growth and

survival of L. vannamei. These might be due to the

synergistic effects of the improved water quality,

higher bacterial and zooplankton densities. Studies

have indicated that carbohydrate addition can

result in the production and accumulation of bio-

flocs (Avnimelech 2007; Emerenciano, Ballester,

Cavalli & Wasielesky 2011; Gao, Shan, Zhang,

Bao & Ma 2012), which could serve as an impor-

tant food source for the zooplankton and thus

could increase the growth of the shrimp. It has

been demonstrated that zooplankton serve as a

supplemental food source for L. vannamei (Chen &

Chen 1992) and therefore could, increase the con-

version efficiency of microbial protein into L. van-

namei protein. Studies have also demonstrated that

bioflocs serve as a good source of protein for

shrimp and lower the demand for feed protein (Ta-

con, Cody, Conquest, Divakaran, Forster & Decamp

2002; Burford & Lorenzen 2004). Avnimelech,

Verdegem, Kurup and Keshavanath (2008) also

demonstrated that carbohydrate addition can lead

to increase in protein utilization and supply of

essential lipids and vitamins for the growth of

shrimp.

Biochemical composition of shrimp

The bio chemical composition of shrimp depends

on the proximate value of the biofloc. It seems that

the higher crude protein was observed in all bio-

floc treatments ranges from 20% to 21.6% and

low CP observed in control. The shrimps cultured

in the biofloc system have more nutritional quality

than the shrimps reared in the control system. It

was confirmed that presence of high proximate

composition in the biofloc leads to better growth of

shrimp. The proximate composition of L. vannamei

was similar to the observation made by Xu and

Pan (2012).

Biochemical and nutrient composition of biofloc

The biochemical and nutrient composition of the

biofloc, derived from biofloc tanks, fed with differ-

ent carbon sources, were significantly different

with regard to all the nutritional parameters

between the treatments and control, indicating the

importance of carbon source. In the study, the

high protein content was observed in the biofloc

produced in the treatment BFTW and BFTT fol-

lowed by BFTS (45.98%). Biofloc that contains

more than 50% crude protein, 4% fibre, 7% ash

and 22 kJ g�1 energy on dry matter basis can be

considered as appropriate in fish nutrition espe-

cially for herbivorous/omnivorous fish and shrimp

species (Webster & Lim 2002). It was confirmed

that the biofloc produced in the study provided

good nutrition to the shrimp. Proximate composi-

tions of the bioflocs from the current experiment

revealed that they contained appropriate level of

crude protein and crude lipid for omnivorous

L. vannamei (Cuzon, Lawrence, Gaxiola, Rosas &

Guillaume 2004). The biofloc was able to provide

sufficient nutrient content for growth of the

shrimp. The nutrient composition (Fe, Zn, Ca, Mg,

Na, K and total phosphorus), observed in the bio-

floc, were similar to the nutrient composition

observed by Kuhn et al. (2010). The higher nutri-

ent level of Ca and Fe was observed in the biofloc

treatment BFTT, whereas Mg, Na and K in BFTW.

The C/N ratio of the biofloc was inversely propor-

tional to the protein content of the biofloc. If the

protein content of the biofloc is high, the C/N ratio

is low.

Conclusions

This study evaluated the biofloc effect of biofloc on

growth of L. vannamei, water quality and biofloc

composition. Among the biofloc system, BFTWeffectively reduced the total ammonia-nitrogen

while maintaining good water quality for shrimp

culture. The use of wheat flour (BFTW) for the bio-

floc production could effectively enhance the bio-

floc production and contributed towards good

water quality which resulted in higher production

of shrimp. The wheat flour has easily digestible

and available carbon for the growth of microor-

ganism. Hence, the microorganisms easily assimi-

lated and multiplied faster than other treatments.

The higher nutritional value of the biofloc devel-

oped by wheat flour would have increased the

growth of L. vannamei than other treatments. In

generally, the biofloc system would increase

growth rates of L. vannamei as the shrimps that

feed on the biofloc would get the additional supple-

ment nutrition from the assimilated nutritious

planktons, bacteria and organic compounds. From



the results of this study, it is confirmed that biofloc

provided sufficient nutrition leads to the growth of

shrimp. This system can play a key role in devel-

oping a sustainable aquaculture via better water

quality maintenance decrease in feed requirements

and higher production to achieve more profit in

shrimp farming.

Acknowledgments

The authors acknowledge the Indian Council of

Agricultural Research and Central Institute of

Fisheries Education, India for the financial support

in the execution of this work. We express our sin-

cere thanks to Dr W. S. Lakra, Director, CIFE,

Mumbai for his kind support extended during the

study period. The first author is grateful to Mr A.

K. Padmanabhan, Mr K. K. Anas, Mr C. Gunasek-

aran, Mr T. Sivaramakrishnan, Ms L. Remya, Ms

Ramya Raj and Mr Ratheesh Kumar for the help

extended during the study.

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